Abstract
Nonpharmaceutical interventions (NPIs) have been commonly deployed to prevent and control the spread of the coronavirus disease 2019 (COVID-19), resulting in a worldwide decline in influenza prevalence. However, the influenza risk in China warrants cautious assessment. We conducted a cross-sectional, seroepidemiological study in Shandong Province, Northern China in mid-2021. Hemagglutination inhibition was performed to test antibodies against four influenza vaccine strains. A combination of descriptive and meta-analyses was adopted to compare the seroprevalence of influenza antibodies before and during the COVID-19 pandemic. The overall seroprevalence values against A/H1N1pdm09, A/H3N2, B/Victoria, and B/Yamagata were 17.8% (95% CI 16.2%–19.5%), 23.5% (95% CI 21.7%–25.4%), 7.6% (95% CI 6.6%–8.7%), and 15.0 (95% CI 13.5%–16.5%), respectively, in the study period. The overall vaccination rate was extremely low (2.6%). Our results revealed that antibody titers in vaccinated participants were significantly higher than those in unvaccinated individuals (P < 0.001). Notably, the meta-analysis showed that antibodies against A/H1N1pdm09 and A/H3N2 were significantly low in adults after the COVID-19 pandemic (P < 0.01). Increasing vaccination rates and maintaining NPIs are recommended to prevent an elevated influenza risk in China.
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Anderson ML, Dobkin C, Gorry D. Effect of influenza vaccination for the elderly on hospitalization and mortality. Ann Intern Med 2020; 173(4): 322–323
Xu C, Liu L, Ren B, Dong L, Zou S, Huang W, Wei H, Cheng Y, Tang J, Gao R, Feng L, Zhang R, Yuan C, Wang D, Chen J. Incidence of influenza virus infections confirmed by serology in children and adult in a suburb community, northern China, 2018–2019 influenza season. Influenza Other Respir Viruses 2021; 15(2): 262–269
Tam YH, Valkenburg SA, Perera RAPM, Wong JHF, Fang VJ, Ng TWY, Kwong ASK, Tsui WWS, Ip DKM, Poon LLM, Chau CKV, Barr IG, Peiris JSM, Cowling BJ. Immune responses to twice-annual influenza vaccination in older adults in Hong Kong. Clin Infect Dis 2018; 66(6): 904–912
Shu LM, Zhang J, Huo X, Chen C, Fang SS, Zong KX, Guo YY, Zhao YZ, Zhang J, Bao CJ, Xia JJ, Zhu FC, Wang DY, Wu GZ, Gao F, Liu J. Preplanned studies: surveillance on the immune effectiveness of quadrivalent and trivalent split influenza vaccines — Shenzhen City and Changzhou City, China, 2018–2019. China CDC Wkly 2020; 2(21): 370–375
Zhu H, Lee ACY, Li C, Mak WWN, Chen YY, Chan KH, Zhang AJX, Fung WF, Zhang RQ, Fung YF, Poon RWS, Lam JY, Tam S, Hung IFN, Chen H, Yuen KY, To KKW. Low population serum microneutralization antibody titer against the predominating influenza A(H3N2) N121K virus during the severe influenza summer peak of Hong Kong in 2017. Emerg Microbes Infect 2018; 7(1): 23
National Health Commission of the People’s Republic of China. Overview of the national epidemic of statutory infectious diseases. 2019. Available at the website of National Health Commission of the People’s Republic of China (accessed December 28, 2021)
Feng S, Shen C, Xia N, Song W, Fan M, Cowling BJ. Rational use of face masks in the COVID-19 pandemic. Lancet Respir Med 2020; 8(5): 434–436
Prather KA, Wang CC, Schooley RT. Reducing transmission of SARS-CoV-2. Science 2020; 368(6498): 1422–1424
Leung NHL, Chu DKW, Shiu EYC, Chan KH, McDevitt JJ, Hau BJP, Yen HL, Li Y, Ip DKM, Peiris JSM, Seto WH, Leung GM, Milton DK, Cowling BJ. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat Med 2020; 26(5): 676–680
Han S, Zhang T, Lyu Y, Lai S, Dai P, Zheng J, Yang W, Zhou X, Feng L. The incoming influenza season — China, the United Kingdom, and the United States, 2021–2022. China CDC Wkly 2021; 3(49): 1039–1045
World Health Organization. Review of global influenza circulation, late 2019 to 2020, and the impact of the COVID-19 pandemic on influenza circulation. 2021. Available at the website of World Health Organization (accessed December 28, 2021)
Zhang AJ, Lee ACY, Chan JFW, Liu F, Li C, Chen Y, Chu H, Lau SY, Wang P, Chan CCS, Poon VKM, Yuan S, To KKW, Chen H, Yuen KY. Coinfection by severe acute respiratory syndrome coronavirus 2 and influenza A(H1N1)pdm09 virus enhances the severity of pneumonia in golden syrian hamsters. Clin Infect Dis 2021; 72(12): e978–e992
Bai L, Zhao Y, Dong J, Liang S, Guo M, Liu X, Wang X, Huang Z, Sun X, Zhang Z, Dong L, Liu Q, Zheng Y, Niu D, Xiang M, Song K, Ye J, Zheng W, Tang Z, Tang M, Zhou Y, Shen C, Dai M, Zhou L, Chen Y, Yan H, Lan K, Xu K. Coinfection with influenza A virus enhances SARS-CoV-2 infectivity. Cell Res 2021; 31(4): 395–403
Cuadrado-Payán E, Montagud-Marrahi E, Torres-Elorza M, Bodro M, Blasco M, Poch E, Soriano A, Piñeiro GJ. SARS-CoV-2 and influenza virus co-infection. Lancet 2020; 395(10236): e84
Yang J, Atkins KE, Feng L, Pang M, Zheng Y, Liu X, Cowling BJ, Yu H. Seasonal influenza vaccination in China: landscape of diverse regional reimbursement policy, and budget impact analysis. Vaccine 2016; 34(47): 5724–5735
Hayward AC, Fragaszy EB, Bermingham A, Wang L, Copas A, Edmunds WJ, Ferguson N, Goonetilleke N, Harvey G, Kovar J, Lim MSC, McMichael A, Millett ERC, Nguyen-Van-Tam JS, Nazareth I, Pebody R, Tabassum F, Watson JM, Wurie FB, Johnson AM, Zambon M; Flu Watch Group. Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study. Lancet Respir Med 2014; 2(6): 445–454
Ma M, Anderson BD, Wang T, Chen Y, Zhang D, Gray GC, Lu J. Serological evidence and risk factors for swine influenza infections among Chinese swine workers in Guangdong Province. PLoS One 2015; 10(5): e0128479
Ng TWY, Perera RAPM, Fang VJ, Yau EM, Peiris JSM, Tam YH, Cowling BJ. The effect of influenza vaccination history on changes in hemagglutination inhibition titers after receipt of the 2015–2016 influenza vaccine in older adults in Hong Kong. J Infect Dis 2020; 221(1): 33–41
Gao D, Yang H, Deng B, Yin G, Song W, Zhang H, Li Y. Safety and immunogenicity of 3 seasonal trivalent influenza vaccines in the Chinese military. Hum Vaccin Immunother 2016; 12(10): 2634–2639
Wang SY, Liu SZ, Chu K, Zhao Y, Zhu FC, Hu YM, Meng FY, Li JX, Luo L, Yang JY, Liu P, Yu J. Immunogenicity and safety of an inactivated quadrivalent influenza vaccine candidate versus inactivated trivalent influenza vaccines in participants >/=3 years of age: a double-blind, randomized, parallel-controlled phase III clinical trial in China. Expert Rev Vaccines 2017; 16(11): 1155–1169
Chen J, Ma J, White SK, Cao Z, Zhen Y, He S, Zhu W, Ke C, Zhang Y, Su S, Zhang G. Live poultry market workers are susceptible to both avian and swine influenza viruses, Guangdong Province, China. Vet Microbiol 2015; 181(3–4): 230–235
Wang JR, Guan WD, Yau LF, Gao WN, Zhan YQ, Liu L, Yang ZF, Jiang ZH. Glycomic signatures on serum IgGs for prediction of postvaccination response. Sci Rep 2015; 5(1): 7648
Quan C, Wang Q, Zhang J, Zhao M, Dai Q, Huang T, Zhang Z, Mao S, Nie Y, Liu J, Xie Y, Zhang B, Bi Y, Shi W, Liu P, Wang D, Feng L, Yu H, Liu WJ, Gao GF. Avian influenza A viruses among occupationally exposed populations, China, 2014–2016. Emerg Infect Dis 2019; 25(12): 2215–2225
Wu J, Yi L, Ni H, Zou L, Zhang H, Zeng X, Liang L, Li L, Zhong H, Zhang X, Lin JY, Ke C. Anti-human H1N1pdm09 and swine H1N1 virus antibodies among swine workers in Guangdong Province, China. Sci Rep 2015; 5(1): 12507
Chinese National Influenza Center. Chinese influenza weekly report. 2021. Available at the website of Chinese National Influenza Center (accessed December 28, 2021)
University of Oxford. Coronavirus (COVID-19) vaccinations. 2021. Available at the ourworldindata website (accessed December 28, 2021)
World Health Organization. Global circulation of influenza viruses. 2021. Available at the website of World Health Organization (accessed December 28, 2021)
Acknowledgements
We thank the participants of this study, as well as the staff of the Second Affiliated Hospital of Shandong First Medical University and Boshan District Hospital who made the survey possible. We thank the help from Ti Liu and Julong Wu in Shandong Center for Disease Control and Prevention. This work was supported by the Academic Promotion Programme of Shandong First Medical University (No. 2019QL006) and the Natural Science Foundation of Shandong Province (Nos. ZR2020QH133, ZR2020MH339, and ZR2021MC001).
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Chuansong Quan, Zhenjie Zhang, Guoyong Ding, Fengwei Sun, Hengxia Zhao, Qinghua Liu, Chuanmin Ma, Jing Wang, Liang Wang, Wenbo Zhao, Jinjie He, Yu Wang, Qian He, Michael J. Carr, Dayan Wang, Qiang Xiao, and Weifeng Shi declare that they have no actual or potential competing financial interests. This study was approved by the Ethics Committee of Shandong First Medical University & Shandong Academy of Medical Sciences (approved No. R202105170154). The study conformed to the principles of the Declaration of Helsinki, and the standards of Good Clinical Practice defined by the International Conference on Harmonization. Written informed consent was obtained from all adult participants, and from legal guardians for participants ≤ 15 years old.
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Quan, C., Zhang, Z., Ding, G. et al. Seroprevalence of influenza viruses in Shandong, Northern China during the COVID-19 pandemic. Front. Med. 16, 984–990 (2022). https://doi.org/10.1007/s11684-022-0930-5
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DOI: https://doi.org/10.1007/s11684-022-0930-5